Skip to main content
SpringerLink
Log in

Influence of polystyrene microplastics on rotifer (Brachionus calyciflorus) growth, reproduction, and antioxidant responses

  • Published:
Aquatic Ecology Aims and scope Submit manuscript

Abstract

Most aquatic environments are suffering from microplastic pollution, which poses a threat to the physiological and ecological characteristics of aquatic animals. The phospholipid hydroperoxide glutathione peroxidase gene (PHGPx) has an important function in the antioxidative defense of organisms. Here, we revealed for the first time that the full-length cDNA of PHGPx in Brachionus calyciflorus was 817 bp long and contained a 512 bp open reading frame. B. calyciflorus was exposed to 0 (control), 1 × 104, 1 × 105, 1 × 106, and 1 × 107 particles mL−1 polystyrene (particle size: 1 µm). Specific growth rate (SGR); reproductive rate (R); superoxide dismutase (SOD), catalase (CAT), and PHGPx activities; manganese superoxide dismutase (MnSOD), copper and zinc superoxide dismutase (CuZnSOD), CAT, and PHGPx expression; and reactive oxygen species (ROS) levels were investigated. Our results showed that polystyrene enhanced ROS production. SGR, R, PHGPx activity, and PHGPx expression decreased with the increase in polystyrene concentrations. SOD and CAT activities and MnSOD, CuZnSOD, and CAT expression levels increased upon exposure to 1 × 104–1 × 106 particles mL−1 polystyrene but decreased under exposure to 1 × 107 particles mL−1 polystyrene. These results revealed that PHGPx, MnSOD, CuZnSOD, and CAT expression regulates antioxidant enzyme activities, which are involved in the PHGPx-associated antioxidant defense of rotifers in response to polystyrene.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • ASTM (2001) Standard guide for acute toxicity tests with the rotifer Brachionus. Annual book of ASTM standards, water and environmental technology, vol. 1105. Biological effects and environmental fates. American Society for Testing and Materials, West Conshohocken

  • Avio CG, Gorbi S, Milan M, Benedetti M, Fattorini D, d’Errico G, Pauletto M, Bargelloni L, Regoli F (2015) Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environ Pollut 198:211–222

    Article  CAS  PubMed  Google Scholar 

  • Backhaus T, Wagner M (2020) Microplastics in the environment: much ado about nothing? A Debate. Glob Chall 4:1900022

    Article  PubMed  Google Scholar 

  • Batel A, Linti F, Scherer M, Erdinger L, Braunbeck T (2016) Transfer of benzo[a]pyrene from microplastics to Artemia nauplii and further to zebrafish via a trophic food web experiment: CYP1A induction and visual tracking of persistent organic pollutants. Environ Toxicol Chem 35:1656–1666

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Chen JC, Chen MY, Fang C, Zheng RH, Jiang YL, Zhang YS, Wang KJ, Bailey C, Segner H, Bo J (2020) Microplastics negatively impact embryogenesis and modulate the immune response of the marine medaka Oryzias melastigma. Mar Poll Bull 158:111349

    Article  CAS  Google Scholar 

  • De Almeida EA, Miyamoto S, Bainy ACD, De Medeiros MHG, Di Mascio P (2004) Protective effect of phospholipid hydroperoxide glutathione peroxidase (PHGPx) against lipid peroxidation in mussels perna exposed to different metals. Mar Poll Bull 49:386–392

    Article  CAS  Google Scholar 

  • Eriksen M, Mason S, Wilson S, Box C, Zellers A, Edwards W, Farley H, Amato S (2013) Microplastic pollution in the surface waters of the Laurentian great lakes. Mar Pollut Bull 77:177–182

    Article  CAS  PubMed  Google Scholar 

  • Foley CJ, Feiner ZS, Malinich TD, Höök TO (2018) A meta-analysis of the effects of exposure to microplastics on fish and aquatic invertebrates. Sci Total Environ 631–632:550–559

    Article  PubMed  CAS  Google Scholar 

  • Horn DA, Granek EF, Steele CL (2020) Effects of environmentally relevant concentrations of microplastic fibers on Pacific mole crab (Emerita analoga) mortality and reproduction. Limnol Oceanogr Lett 5:74–83

    Article  Google Scholar 

  • Horton AA, Walton A, Spurgeon DJ, Lahive E, Svendsen C (2017) Microplastics in freshwater and terrestrial environments: evaluating the current understanding to identify the knowledge gaps and future research priorities. Sci Total Environ 586:127–141

    Article  CAS  PubMed  Google Scholar 

  • Imai H, Nakagawa Y (2003) Biological significance of phospholipid hydroperoxide glutathione peroxidase (PHGPx, GPx4) in mammalian cells. Free Radical Biol Med 34:145–169

    Article  CAS  Google Scholar 

  • Iwaoka M, Katakura A, Mishima J, Ishihara Y, Kunwar A, Priyadarsini KI (2015) Mimicking the lipid peroxidation inhibitory activity of phospholipid hydroperoxide glutathione peroxidase (GPx4) by using fatty acid conjugates of a water-soluble selenolane. Molecules 20:12364–12375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong CB, Won EJ, Kang HM, Lee MC, Hwang DS, Hwang UK, Zhou B, Souissi S, Lee SJ, Lee JS (2016) Microplastic size-dependent toxicity, oxidative stress induction, and p-JNK and p-p38 activation in the monogonont rotifer (Brachionus koreanus). Environ Sci Technol 50:8849–8857

    Article  CAS  PubMed  Google Scholar 

  • Lampert W, Trubetskova I (1996) Juvenile growth rate as a measure of fitness in Daphnia. Funct Ecol 10:631–635

    Article  Google Scholar 

  • Lasee S, Maurício J, Thompson WA, Karnjanapiboonwong A, Kasumba J, Subbiah S, Morse A, Anderson TA (2017) Microplastics in a freshwater environment receiving treated wastewater effluent. Integr Environ Assess Manag 13:528–532

    Article  CAS  PubMed  Google Scholar 

  • Lee KW, Shim WJ, Kwon OY, Kang JH (2013) Size-dependent effects of micro polystyrene particles in the marine copepod Tigriopus japonicus. Environ Sci Technol 47:11278–11283

    Article  CAS  PubMed  Google Scholar 

  • Li F, Wang P, Zhao C, Bao W, Qiu L (2017) Cloning and characterization of PHGPx and its synergistic role with p53 in mediating stress in Penaeus monodon. Fish Shellfish Immunol 71:380–392

    Article  CAS  PubMed  Google Scholar 

  • Liang Y, Chen X, Lu X, Jin S, Min Y, Yang J (2017) Combined effects of microcystin and nitrite on the growth, lipid peroxidation, and antioxidant responses of the freshwater rotifer Brachionus calyciflorus. Aquat Toxicol 192:78–88

    Article  CAS  PubMed  Google Scholar 

  • Liang Y, Shao L, Jiang Q, Yang J (2020) Changes in the life-cycle parameters and glutathione-related antioxidant defense system of rotifer Brachionus calyciflorus under the combined stress of microcystin-LR and ammonia. Aquat Ecol 54:243–256

    Article  CAS  Google Scholar 

  • Liu Z, Cai M, Yu P, Chen M, Wu D, Zhang M, Zhao Y (2018) Age-dependent survival, stress defense, and AMPK in Daphnia pulex after short-term exposure to a polystyrene nanoplastic. Aquat Toxicol 204:1–8

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Yu P, Cai M, Wu D, Zhang M, Huang Y, Zhao Y (2019) Polystyrene nanoplastic exposure induces immobilization, reproduction, and stress defense in the freshwater cladoceran Daphnia pulex. Chemosphere 215:74–81

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Manfra L, Rotini A, Bergami E, Grassi G, Faleri C, Corsi I (2017) Comparative ecotoxicity of polystyrene nanoparticles in natural seawater and reconstituted seawater using the rotifer Brachionus plicatilis. Ecotox Environ Safe 145:557–563

    Article  CAS  Google Scholar 

  • Mattsson K, Hansson LA, Cedervall T (2015) Nano-plastics in the aquatic environment. Environ Sci Process Impacts 17:1712–1721

    Article  CAS  PubMed  Google Scholar 

  • Messinetti S, Mercurio S, Parolini M, Sugni M, Pennati R (2018) Effects of polystyrene microplastics on early stages of two marine invertebrates with different feeding strategies. Environ Pollut 237:1080–1087

    Article  CAS  PubMed  Google Scholar 

  • Moore CJ, Lattin GL, Zellers AF (2011) Quantity and type of plastic debris flowing from two urban rivers to coastal waters and beaches of Southern California. J Integr Coast Zone Manag 11:65–73

    Google Scholar 

  • Ogonowski M, Schur C, Jarsen A, Gorokhova E (2016) The effects of natural and anthropogenic microparticles on individual fitness in Daphnia magna. PloS One 11:e0155063

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pacitti D, Wang T, Page MM, Martin SAM, Sweetman J, Feldmann J, Secombes CJ (2013) Characterization of cytosolic glutathione peroxidase and phospholipid-hydroperoxide glutathione peroxidase genes in rainbow trout (Oncorhynchus mykiss) and their modulation by in vitro selenium exposure. Aquat Toxicol 130–131:97–111

    Article  PubMed  CAS  Google Scholar 

  • Park JC, Han J, Lee MC, Seo JS, Lee JS (2017) Effects of triclosan (TCS) on fecundity, the antioxidant system, and oxidative stress-mediated gene expression in the copepod Tigriopus japonicas. Aquat Toxicol 189:16–24

    Article  CAS  PubMed  Google Scholar 

  • Peng G, Xu P, Zhu B, Bai M, Li D (2018) Microplastics in freshwater river sediments in Shanghai, China: a case study of risk assessment in mega-cities. Environ Pollut 234:448–456

    Article  CAS  PubMed  Google Scholar 

  • Rehse S, Kloas W, Zarfl C (2016) Short-term exposure with high concentrations of pristine microplastic particles leads to immobilization of Daphnia magna. Chemosphere 153:91–99

    Article  CAS  PubMed  Google Scholar 

  • Rochman CM, Brookson C, Bikker J, Djuric N, Earn A, Bucci K, Athey S, Huntington A, Mcllwraith H, Munno K, De Frond H, Kolomijeca A, Erdle L, Grbic J, Bayoumi M, Borrelle SB, Wu T, Santoro S, Werbowski LM, Zhu X, Giles RK, Hamilton BM, Thaysen C, Kaura A, Klasios N, Ead L, Kim J, Sherlock C, Ho A, Hung C (2019) Rethinking microplastics as a diverse contaminant suite. Environ Toxicol Chem 38:703–711

    Article  CAS  PubMed  Google Scholar 

  • Shah JA, Pandit AK, Shah GM (2015) A research on rotifers of aquatic ecosystems of Kashmir Himalaya for documentation and authentication. Proc Natl Acad Sci India Sect B Biol Sci 85:13–19

    Article  Google Scholar 

  • Snell TW (1980) Blue-green algae and selection in rotifer populations. Oecologia 46:343–346

    Article  PubMed  Google Scholar 

  • Snell TW, Janssen CR (1995) Rotifers in ecotoxicology: a review. Hydrobiologia 313(314):231–247

    Article  Google Scholar 

  • Snell TW, Joaquim-Justo C (2007) Workshop on rotifers in ecotoxicology. Hydrobiologia 593:227–232

    Article  Google Scholar 

  • Snell TW, Moffat BD (1992) A 2-d life cycle test with the rotifer Brachionus calyciflorus. Environ Toxicol Chem 11:1249–1257

    Article  CAS  Google Scholar 

  • Strungaru SA, Jijie R, Nicoara M, Plavan G, Faggio C (2019) Micro-(nano) plastics in freshwater ecosystems: Abundance, toxicological impact and quantification methodology. Trends Anal Chem 110:116–128

    Article  CAS  Google Scholar 

  • Sun X, Chen B, Li Q, Liu N, Xia B, Zhu L, Qu K (2018) Toxicities of polystyrene nano- and microplastics toward marine bacterium Halomonas alkaliphila. Sci Total Environ 642:1378–1385

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Xu W, Gu Q, Chen Y, Zhou Q, Zhang L, Gu L, Huang Y, Lyu K, Yang Z (2019) Small-sized microplastics negatively affect rotifers: changes in the key life-history traits and rotifer-Phaeocystis population dynamics. Environ Sci Technol 53:9241–9251

    Article  CAS  PubMed  Google Scholar 

  • Sussarellu R, Suquet M, Thomas Y, Lambert C, Fabioux C, Pernet MEJ, Le Goïc N, Quillien V, Mingant C, Epelboin Y, Corporeau C, Guyomarch J, Robbens J, Paul-Pont I, Soudant P, Huvet A (2016) Oyster reproduction is affected by exposure to polystyrene microplastics. Proc Natl Acad Sci 113:2430–2435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang J, Wang X, Yin J, Han Y, Yang J, Lu X, Xie T, Akbar S, Lyu K, Yang Z (2019) Molecular characterization of thioredoxin reductase in waterflea Daphnia magna and its expression regulation by polystyrene microplastics. Aquat Toxicol 208:90–97

    Article  CAS  PubMed  Google Scholar 

  • Uye S (1982) Length-weight relationships of important zooplankton from the inland sea of Japan. J Oceanogr Soc Jpn 38:149–158

    Article  Google Scholar 

  • Wang H, Tang X, Sha J, Chen H, Sun T, Wang Y (2015) The reproductive toxicity on the rotifer Brachionus plicatilis induced by BDE-47 and studies on the effective mechanism based on antioxidant defense system changes. Chemosphere 135:129–137

    Article  CAS  PubMed  Google Scholar 

  • Wen B, Jin SR, Chen ZZ, Gao JZ, Liu YN, Liu JH, Feng XS (2018) Single and combined effects of microplastics and cadmium on the cadmium accumulation, antioxidant defense and innate immunity of the discus fish (Symphysodon aequifasciatus). Environ Pollut 243:462–471

    Article  CAS  PubMed  Google Scholar 

  • Yagi K, Shidoji Y, Komura S, Kojima H, Ohishi N (1998) Dissipation of mitochondrial membrane potential by exogenous phospholipid monohydroperoxide and protection against this effect by transfection of cells with phospholipid hydroperoxide glutathione peroxidase gene. Biochem Biophys Res Commun 245:528–533

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Dong S, Jiang Q, Kuang T, Huang W, Yang J (2013) Changes in expression of manganese superoxide dismutase, copper and zinc superoxide dismutase and catalase in Brachionus calyciflorus during the aging process. PLoS One 8:e57186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang D, Shi H, Li I, Li J, Jabeen K, Kolandhasamy P (2015) Microplastic pollution in table salts from China. Environ Sci Technol 49:13622–13627

    Article  CAS  PubMed  Google Scholar 

  • Yu P, Liu Z, Wu D, Chen M, Lv W, Zhao Y (2018) Accumulation of polystyrene microplastics in juvenile Eriocheir sinensis and oxidative stress effects in the liver. Aquat Toxicol 200:28–36

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, He Y, He L, Zong HY, Cai GB (2015) Molecular cloning and characterization of a phospholipid hydroperoxide glutathione peroxidase gene from a blood fluke Schistosoma japonicum. Mol Biochem Parasit 142:1595–1604

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Natural Science Foundation of the Jiangsu Higher Education Institutions of China (Grant number: 19KJB180020), the Fund of Fujian Provincial Key Laboratory of Marine Ecological Conservation and Restoration (Grant number: EPR2020004), and the Startup Foundation for Introducing Talent of NUIST (Grant numbers: 2018r040 and 2020r062).

Author information

Authors and Affiliations

  1. School of Marine Sciences, Nanjing University of Information Science & Technology, No. 219 Ningliu Road, Nanjing, 210044, People’s Republic of China

    Ye Liang, Xiaotong Yang, Yishan Wang, Rui Liu, Haifeng Gu & Longjiang Mao

  2. Fujian Provincial Key Laboratory of Marine Ecological Conservation and Restoration, No. 178 Daxue Road, Xiamen, 361005, People’s Republic of China

    Ye Liang & Haifeng Gu

Authors
  1. Ye Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaotong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yishan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rui Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Haifeng Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Longjiang Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Haifeng Gu or Longjiang Mao.

Ethics declarations

Conflict of interest

The authors declare that they do not have any conflict of interest.

Ethical approval

All applicable international, national, and institutional guidelines for the use of animals were followed by the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Handling Editor: Télesphore Sime-Ngando

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liang, Y., Yang, X., Wang, Y. et al. Influence of polystyrene microplastics on rotifer (Brachionus calyciflorus) growth, reproduction, and antioxidant responses. Aquat Ecol 55, 1097–1111 (2021). https://doi.org/10.1007/s10452-021-09885-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10452-021-09885-y

Keywords

Search

Navigation